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High flavonoid-producing tomato reduces whitefly phloem-feeding efficiency by inducing reactive oxygen species accumulation and callose deposition

Published online by Cambridge University Press:  27 June 2025

Yujie Li ,
Tianyu Huang ,
Fengbo Yang ,
Rong Zhang ,
Weina Gu ,
Peng Lu ,
Hong Tong ,
Yuting Yang ,
Zhixiong Zhou  and
Qingjun Wu
...Show all authors
Yujie Li
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China
Tianyu Huang
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China
Fengbo Yang
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China
Rong Zhang
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China State Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, China
Weina Gu
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China State Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, China
Peng Lu
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China
Hong Tong
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China
Yuting Yang
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China
Zhixiong Zhou
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China
Qingjun Wu
Affiliation:
State Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, China
Youjun Zhang
Affiliation:
State Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, China
Qi Su*
Affiliation:
Ministry of Agriculture and Rural Affairs Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-construction by Ministry and Province), Hubei Engineering Technology Center for Forewarning and Management of Agricultural and Forestry Pests, College of Agriculture, Yangtze University, Jingzhou, China
*
Corresponding author: Qi Su; Email: qsu@yangtzeu.edu.cn
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Abstract

The whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) is economically one of the most threatening pests in tomato cultivation, which not only causes direct damage but also transmits many viruses. Breeding whitefly-resistant tomato varieties is a promising and environmentally friendly method to control whitefly populations in the field. Accumulating evidence from tomato and other model systems demonstrates that flavonoids contribute to plant resistance to herbivorous insects. Previously, we found that high flavonoid-producing tomato line deterred whitefly oviposition and settling behaviours, and was more resistant to whiteflies compared to the near-isogenic low flavonoid-producing tomato line. The objective of the current work is to describe in detail different aspects of the interaction between the whitefly and two tomato lines, including biochemical processes involved. Electrical penetration graph recordings showed that high flavonoid-producing tomato reduced whitefly probing and phloem-feeding efficiency. We also studied constitutive and induced plant defence responses and found that whitefly induced stronger reactive oxygen species accumulation through NADPH oxidase in high flavonoid-producing tomato than in low flavonoid-producing tomato. Moreover, whitefly feeding induced the expression of callose synthase genes and resulted in callose deposition in the sieve elements in high flavonoid-producing tomato but not in low flavonoid-producing tomato. As a consequence, whitefly feeding on high flavonoid-producing tomato significantly decreased uptake of phloem and reduced its performance when compared to low flavonoid-producing tomato. These results indicate that high flavonoid-producing tomato provides phloem-based resistance against whitefly infestation and that the breeding of such resistance in new varieties could enhance whitefly management.

Keywords

callose depositionplant immunityROS accumulationSolanum lycopersicumwhitefly resistance

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Research Paper
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Bulletin of Entomological Research , First View , pp. 1 - 9
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© The Author(s), 2025. Published by Cambridge University Press.

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References

Adkar-Purushothama, CR, Brosseau, C, Giguere, T, Sano, T, Moffett, P and Perreault, JP (2015) Small RNA derived from the virulence modulating region of the potato spindle tuber viroid silences callose synthase genes of tomato plants. Plant Cell 27, 2178–2194.10.1105/tpc.15.00523CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.10.1016/0003-2697(76)90527-3CrossRefGoogle ScholarPubMed
Depalo, L, Gallego, C, Ortells-Fabra, R, Salas, C, Montalt, R, Urbaneja, A and Pérez-Hedo, M (2024) Advancing tomato crop protection: Green leaf volatile-mediated defense mechanisms against Nesidiocoris tenuis plant damage. Biological Control 192, 105517.10.1016/j.biocontrol.2024.105517CrossRefGoogle Scholar
De Vos, M, Van Oosten, VR, Van Poecke, RM, Van Pelt, JA, Pozo, MJ, Mueller, MJ, Buchala, AJ, Métraux, JP, Van Loon, L and Dicke, M (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions 18, 923–937.10.1094/MPMI-18-0923CrossRefGoogle ScholarPubMed
Elbaz, M, Halon, E, Malka, O, Malitsky, S, Blum, E and Aharoni, A (2012) Asymmetric adaptation to indolic and aliphatic glucosinolates in the B and Q sibling species of Bemisia tabaci (Hemiptera: Aleyrodidae). Molecular Ecology 21, 4533–4546.10.1111/j.1365-294X.2012.05713.xCrossRefGoogle Scholar
Escobar-Bravo, R, Alba, JM, Pons, C, Granell, A, Kant, MR and Moriones, E (2016) A jasmonate-inducible defense trait transferred from wild into cultivated tomato establishes increased whitefly resistance and reduced viral disease incidence. Frontiers in Plant Science 7, 1732.10.3389/fpls.2016.01732CrossRefGoogle ScholarPubMed
Fereres, A and Moreno, A (2009) Behavioral aspects influencing plant virus transmission by homopteran insects. Virus Research 141, 158–168.10.1016/j.virusres.2008.10.020CrossRefGoogle ScholarPubMed
Forslund, K, Pettersson, J, Bryngelsson, T and Jonsson, L (2000) Aphid infestation induces PR-proteins differently in barley susceptible or resistant to the birdcherry-oat aphid (Rhopalosiphum padi). Physiologia Plantarum 110, 496–502.Google Scholar
Foyer, CH, Rasool, B, Davey, JW and Hancock, RD (2016) Cross-tolerance to biotic and abiotic stresses in plants: A focus on resistance to aphid infestation. Journal of Experimental Botany 67, 2025–2037.10.1093/jxb/erw079CrossRefGoogle ScholarPubMed
Funnell, DL, Lawrence, CB, Pedersen, JF and Schardl, CL (2004) Expression of the tobacco β-1,3-glucanase gene, PR-2d, following induction of SAR with Peronospora tabacina. Physiological and Molecular Plant Pathology 65, 285–296.10.1016/j.pmpp.2005.02.010CrossRefGoogle Scholar
Garzo, E, Fernández-Pascual, M, Morcillo, C, Fereres, A, Gómez-Guillamón, ML and Tjallingii, WF (2018) Ultrastructure of compatible and incompatible interactions in phloem sieve elements during the stylet penetration by cotton aphids in melon. Insect Science 25, 631–642.10.1111/1744-7917.12447CrossRefGoogle ScholarPubMed
Gilbertson, RL, Batuman, O, Webster, CG and Adkins, S (2015) Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis, in the emergence and global spread of plant viruses. Annual Review of Virology 2, 67–93.10.1146/annurev-virology-031413-085410CrossRefGoogle ScholarPubMed
Gouveia, BT, de Oliveira, AMS, Ribeiro, GHMR and Maluf, WR (2018) Resistance to whitefly (Bemisia argentifolii) and repellency to the two-spotted spider mite (Tetranychus urticae) in tomato plant hybrids with high leaf contents of acylsugar and the Mi gene. Euphytica 214, 140.10.1007/s10681-018-2224-1CrossRefGoogle Scholar
Gupta, P, Ravi, I and Sharma, V (2013) Induction of β-1,3-glucanase and chitinase activity in the defense response of Eruca sativa plants against the fungal pathogen Alternaria brassicicola. Journal of Plant Interactions 8, 155–161.10.1080/17429145.2012.679705CrossRefGoogle Scholar
Hao, PY, Liu, CX, Wang, YY, Chen, RZ, Tang, M, Du, B, Zhu, LL and He, GC (2008) Herbivore-induced callose deposition on the sieve plates of rice: An important mechanism for host resistance. Plant Physiology 146, 1810–1820.10.1104/pp.107.111484CrossRefGoogle Scholar
Ho, JY, Weide, R, Ma, HM, Vanwordragen, MF, Lambert, KN and Koornneef, M (1992) The root-knot nematode resistance gene (Mi) in tomato-construction of a molecular linkage map and identification of dominant cDNA markers in resistant genotypes. Plant Journal 2, 971–982.10.1046/j.1365-313X.1992.t01-8-00999.xCrossRefGoogle ScholarPubMed
Horowitz, AR, Ghanim, M, Roditakis, E, Nauen, R and Ishaaya, I (2020) Insecticide resistance and its management in Bemisia tabaci species. Journal of Pest Science 93, 893–910.10.1007/s10340-020-01210-0CrossRefGoogle Scholar
Hosseini-Zahani, F and Parissa, T (2023) The role of oxidative burst, antioxidant genes and enzymes in association with callose in tomato reaction to various taxonomic groups of Rhizoctonia spp. Physiological and Molecular Plant Pathology 128, 102174.10.1016/j.pmpp.2023.102174CrossRefGoogle Scholar
Jacobs, AK, Lipka, V, Burton, RA, Panstruga, R, Strizhov, N, Schulze-Lefert, P and Fincher, GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15, 2503–2513.10.1105/tpc.016097CrossRefGoogle ScholarPubMed
Jiang, YX, De Blas, C, Barrios, L and Fereres, A (2000) Correlation between whitefly (Homoptera: Aleyrodidae) feeding behavior and transmission of tomato yellow leaf curl virus. Annals of the Entomological Society of America 93, 573–579.10.1603/0013-8746(2000)093[0573:CBWHAF]2.0.CO;2CrossRefGoogle Scholar
Jiang, YX, Nombela, G and Muniz, M (2001) Analysis by DC-EPG of the resistance to Bemisia tabaci on an Mi-tomato line. Entomologia Experimentalis et Applicata 99, 295–302.10.1046/j.1570-7458.2001.00828.xCrossRefGoogle Scholar
Jiang, YX and Walker, GP (2007) Identification of phloem sieve elements as the site of resistance to silverleaf whitefly in resistant alfalfa genotypes. Entomologia Experimentalis et Applicata 125, 307–320.10.1111/j.1570-7458.2007.00627.xCrossRefGoogle Scholar
Kempema, LA, Cui, X, Holzer, FM and Walling, LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiology 143, 849–865.10.1104/pp.106.090662CrossRefGoogle ScholarPubMed
Kerchev, PI, Fenton, B, Foyer, CH and Hancock, RD (2012) Infestation of potato (Solanum tuberosum L.) by the peach-potato aphid (Myzus persicae Sulzer) alters cellular redox status and is influenced by ascorbate. Plant Cell and Environment 35, 430–440.10.1111/j.1365-3040.2011.02395.xCrossRefGoogle ScholarPubMed
Knoblauch, M, Froelich, DR, Pickard, WF and Peters, WS (2014) SEORious business: Structural proteins in sieve tubes and their involvement in sieve element occlusion. Journal of Experimental Botany 65, 1879–1893.10.1093/jxb/eru071CrossRefGoogle ScholarPubMed
Kuśnierczyk, A, Winge, P, Jørstad, TS, Troczyńska, J, Rossiter, JT and Bones, AM (2008) Towards global understanding of plant defence against aphids–timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell and Environment 31, 1097–1115.10.1111/j.1365-3040.2008.01823.xCrossRefGoogle ScholarPubMed
Liu, BM, Preisser, EL, Chu, D, Pan, HP, Xie, W, Wang, SL, Wu, QJ and Zhang, YJ (2013) Multiple forms of vector manipulation by a plant-infecting virus: Bemisia tabaci and tomato yellow curl leaf virus. Journal of Virology 87, 4929–4937.10.1128/JVI.03571-12CrossRefGoogle Scholar
Liu, JL, Du, HT, Ding, X, Zhou, YD, Xie, PF and Wu, JC (2017) Mechanisms of callose deposition in rice regulated by exogenous abscisic acid and its involvement in rice resistance to Nilaparvata lugens Stål (Hemiptera: Delphacidae). Pest Management Science 73, 2559–2568.10.1002/ps.4655CrossRefGoogle ScholarPubMed
Liu, XM, Williams, CE, Nemacheck, JA, Wang, HY, Subramanyam, S, Zheng, C and Chen, MS (2010) Reactive oxygen species are involved in plant defense against a gall midge. Plant Physiology 152, 985–999.10.1104/pp.109.150656CrossRefGoogle Scholar
López‐Cruz, J, Crespo‐Salvador, Ó, Fernández‐Crespo, E, García‐Agustín, P and González‐Bosch, C (2017) Absence of Cu–Zn superoxide dismutase BCSOD1 reduces Botrytis cinerea virulence in Arabidopsis and tomato plants, revealing interplay among reactive oxygen species, callose and signalling pathways. Molecular Plant Pathology 18, 16–31.10.1111/mpp.12370CrossRefGoogle ScholarPubMed
Lü, BB, Sun, WW, Zhang, SP, Zhang, CL, Qian, J, Wang, XM, Gao, R and Dong, HS (2011) HrpNEa-induced deterrent effect on phloem feeding of the green peach aphid Myzus persicae requires AtGSL5 and AtMYB44 genes in Arabidopsis thaliana. Journal of Biosciences 36, 123–137.10.1007/s12038-011-9016-2CrossRefGoogle Scholar
Luna, E, Pastor, V, Robert, J, Flors, V, Mauch-Mani, B and Ton, J (2011) Callose deposition: A multifaceted plant defense response. Molecular Plant-Microbe Interactions 24, 183–193.10.1094/MPMI-07-10-0149CrossRefGoogle ScholarPubMed
Maciel, GM, Almeida, RS, da Rocha, JPR, Andaló, V, Marquez, GR and Santos, NC (2017) Mini tomato genotypes resistant to the silverleaf whitefly and to two-spotted spider mites. Genetics and Molecular Research 16, gmr16019539.10.4238/gmr16019539CrossRefGoogle Scholar
Medina-Ortega, KJ and Walker, GP (2015) Faba bean forisomes can function in defence against generalist aphids. Plant Cell and Environment 38, 1167–1177.10.1111/pce.12470CrossRefGoogle ScholarPubMed
Mehrabi, S, Åhman, I and Jonsson, LM (2016) The constitutive expression and induction of three β-1, 3-glucanases by bird cherry-oat aphid in relation to aphid resistance in 15 barley breeding lines. Arthropod-Plant Interactions 10, 101–111.10.1007/s11829-016-9415-2CrossRefGoogle Scholar
Miller, G, Schlauch, K, Tam, R, Cortes, D, Torres, MA and Shulaev, V (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signaling 2, ra45–ra45.10.1126/scisignal.2000448CrossRefGoogle ScholarPubMed
Mittler, R, Vanderauwera, S, Gollery, M and Van Breusegem, F (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490–498.10.1016/j.tplants.2004.08.009CrossRefGoogle ScholarPubMed
Moloi, MJ and van der Westhuizen, AJ (2006) The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. Journal of Plant Physiology 163, 1118–1125.10.1016/j.jplph.2005.07.014CrossRefGoogle ScholarPubMed
Nie, WF, Wang, MM, Xia, XJ, Zhou, YH, Shi, K, Chen, ZX and Yu, JQ (2013) Silencing of tomato RBOH1 and MPK2 abolishes brassinosteroid‐induced H2O2 generation and stress tolerance. Plant Cell and Environment 36, 789–803.10.1111/pce.12014CrossRefGoogle ScholarPubMed
Nombela, G, Beitia, F and Muniz, M (2000) Variation in tomato host response to Bemisia tabaci (Hemiptera: Aleyrodidae) in relation to acyl sugar content and presence of the nematode and potato aphid resistance gene Mi. Bulletin of Entomological Research 90, 161–167.10.1017/S0007485300000274CrossRefGoogle ScholarPubMed
Qiu, ZK, Wang, XX, Gao, JC, Guo, YM, Huang, ZJ and Du, YC (2016) The tomato Hoffman’s anthocyaninless gene encodes a bHLH transcription factor involved in anthocyanin biosynthesis that is developmentally regulated and induced by low temperatures. PLoS One 11, e0151067.10.1371/journal.pone.0151067CrossRefGoogle ScholarPubMed
Riahi, C, Urbaneja, A, Fernández-Muñoz, R, Fortes, IM, Moriones, E and Pérez-Hedo, M (2023) Induction of glandular trichomes to control Bemisia tabaci in tomato crops: Modulation by the natural enemy Nesidiocoris tenuis. Phytopathology 113, 1677–1685.10.1094/PHYTO-11-22-0440-VCrossRefGoogle ScholarPubMed
Rodríguez-López, MJ, Garzo, E, Bonani, JP, Fereres, A, Fernández-Muñoz, R and Moriones, E (2011) Whitefly resistance traits derived from the wild tomato Solanum pimpinellifolium affect the preference and feeding behavior of Bemisia tabaci and reduce the spread of tomato yellow leaf curl virus. Phytopathology 101, 1191–1201.10.1094/PHYTO-01-11-0028CrossRefGoogle ScholarPubMed
Shoala, T, Edwards, MG, Knight, MR and Gatehouse, AM (2018) OXI1 kinase plays a key role in resistance of Arabidopsis towards aphids (Myzus persicae). Transgenic Research 27, 355–366.10.1007/s11248-018-0078-xCrossRefGoogle Scholar
Su, Q, Chen, G, Mescher, MC, Peng, ZK, Xie, W, Wang, SL, Wu, QJ, Liu, J, Li, CR, Wang, WK and Zhang, YJ (2018) Whitefly aggregation on tomato is mediated by feeding-induced changes in plant metabolites that influence the behavior and performance of conspecifics. Functional Ecology 32, 1180–1193.10.1111/1365-2435.13055CrossRefGoogle Scholar
Su, Q, Mescher, MC, Wang, SL, Chen, G, Xie, W, Wu, QJ, Wang, WK and Zhang, YJ (2016) Tomato yellow leaf curl virus differentially influences plant defence responses to a vector and a non-vector herbivore. Plant Cell and Environment 39, 597–607.10.1111/pce.12650CrossRefGoogle Scholar
Su, Q, Peng, ZK, Tong, H, Xie, W, Wang, SL, Wu, QJ and Zhang, YJ (2019) A salivary ferritin in the whitefly suppresses plant defenses and facilitates host exploitation. Journal of Experimental Botany 70, 3343–3355.10.1093/jxb/erz152CrossRefGoogle ScholarPubMed
Su, Q, Preisser, EL, Zhou, XM, Xie, W, Liu, BM, Wang, SL, Wu, QJ and Zhang, YJ (2015) Manipulation of host quality and defense by a plant virus improves performance of whitefly vectors. Journal of Economic Entomology 108, 11–19.10.1093/jee/tou012CrossRefGoogle ScholarPubMed
Su, Q, Yang, FB, Hu, Y, Peng, ZK, Huang, TY, Tong, H, Zhang, R, Yang, YT, Zhou, ZX, Liang, P, Zhu, LH, Wu, QJ, Zhang, YJ and Guo, ZJ (2025) Flavonoids enhance tomato plant resistance to whitefly by interfering with the expression of a salivary effector. Plant Physiology 197, kiaf101.10.1093/plphys/kiaf101CrossRefGoogle ScholarPubMed
Su, Q, Yang, FB, Zhang, QH, Tong, H, Hu, Y, Zhang, XY, Xie, W, Wang, SL, Wu, QJ and Zhang, YJ (2020) Defence priming in tomato by the green leaf volatile (Z)-3-hexenol reduces whitefly transmission of a plant virus. Plant Cell and Environment 43, 2797–2811.10.1111/pce.13885CrossRefGoogle ScholarPubMed
Suhag, A, Yadav, H, Chaudhary, D, Subramanian, S, Jaiwal, R and Jaiwal, PK (2021) Biotechnological interventions for the sustainable management of a global pest, whitefly (Bemisia tabaci). Insect Science 28, 1228–1252.10.1111/1744-7917.12853CrossRefGoogle ScholarPubMed
Sun, MJ, Voorrips, RE, Steenhuis-Broers, G, Van’t Westende, W and Vosman, B (2018) Reduced phloem uptake of Myzus persicae on an aphid resistant pepper accession. BMC Plant Biology 18, 138.10.1186/s12870-018-1340-3CrossRefGoogle Scholar
Sytykiewicz, H (2016) Deciphering the role of NADPH oxidase in complex interactions between maize (Zea mays L.) genotypes and cereal aphids. Biochemical and Biophysical Research Communications 476, 90–95.10.1016/j.bbrc.2016.05.050CrossRefGoogle ScholarPubMed
Tjallingii, WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57, 739–745.10.1093/jxb/erj088CrossRefGoogle ScholarPubMed
Torres, MA (2010) ROS in biotic interactions. Physiologia Plantarum 138, 414–429.10.1111/j.1399-3054.2009.01326.xCrossRefGoogle ScholarPubMed
Urbaneja, A, Ortells-Fabra, R and Pérez-Hedo, M (2024) Enhancing tomato crop resilience to water stress: The role of Trichoderma afroharzianum T22 and Nesidiocoris tenuis management. Entomologia Generalis 44, 1193–1201.10.1127/entomologia/2024/2787CrossRefGoogle Scholar
van den Oever‐van den Elsen, F, Lucatti, AF, van Heusden, S, Broekgaarden, C, Mumm, R, Dicke, M and Vosman, B (2016) Quantitative resistance against Bemisia tabaci in Solanum pennellii: Genetics and metabolomics. Journal of Integrative Plant Biology 58, 397–412.10.1111/jipb.12449CrossRefGoogle ScholarPubMed
Vellosillo, T, Jorge, V, Satish, K, Mats, H and Carmen, C (2010) Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiology 154, 444–448.10.1104/pp.110.161273CrossRefGoogle ScholarPubMed
Verma, DP and Hong, Z (2001) Plant callose synthase complexes. Plant Molecular Biology 47, 693–701.10.1023/A:1013679111111CrossRefGoogle ScholarPubMed
Villada, ES, González, EG, López-Sesé, AI, Castiel, AF and Gómez-Guillamón, ML (2009) Hypersensitive response to Aphis gossypii Glover in melon genotypes carrying the Vat gene. Journal of Experimental Botany 60, 3269–3277.10.1093/jxb/erp163CrossRefGoogle ScholarPubMed
Voigt, CA (2014) Callose-mediated resistance to pathogenic intruders in plant defense-related papillae. Frontiers in Plant Science 5, 168.10.3389/fpls.2014.00168CrossRefGoogle Scholar
Walker, GP and Janssen, JAM (2000) Electronic recording of whitefly (Homoptera: Aleyrodidae) feeding and oviposition behavior. Walker, GP and Backus, EA. (eds.). Principles and Applications of Electronic Monitoring and Other Techniques in the Study of Homopteran Feeding Behavior. Lanham, USA: Entomological Society of America, 172–200.10.4182/EXYL6038CrossRefGoogle Scholar
Xie, B, Wang, X, Zhu, M, Zhang, Z and Hong, Z (2011) CalS7 encodes a callose synthase responsible for callose deposition in the phloem. Plant Journal 65, 1–14.10.1111/j.1365-313X.2010.04399.xCrossRefGoogle ScholarPubMed
Yang, FB, Shen, HW, Huang, TY, Yao, QX, Hu, JY, Tang, J, Zhang, R, Tong, H, Wu, QJ, Zhang, YJ and Su, Q (2023b) Flavonoid production in tomato mediates both direct and indirect plant defences against whiteflies in tritrophic interactions. Pest Management Science 79, 4644–4654.10.1002/ps.7667CrossRefGoogle Scholar
Yang, FB, Zhang, XY, Shen, HW, Xue, H, Tian, T, Zhang, QH, Hu, JY, Tong, H, Zhang, YJ and Su, Q (2023a) Flavonoid-producing tomato plants have a direct negative effect on the zoophytophagous biological control agent Orius sauteri. Insect Science 30, 173–184.10.1111/1744-7917.13085CrossRefGoogle Scholar
Yang, FB, Zhang, XY, Xue, H, Tian, T, Tong, H, Hu, JY, Zhang, R, Tang, J and Su, Q (2022) (Z)-3-hexenol primes callose deposition against whitefly-mediated begomovirus infection in tomato. Plant Journal 112, 694–708.10.1111/tpj.15973CrossRefGoogle ScholarPubMed
Yao, QX, Peng, ZK, Tong, H, Yang, FB, Xing, GS, Wang, LJ, Zheng, JJ, Zhang, YJ and Su, Q (2019) Tomato plant flavonoids increase whitefly resistance and reduce spread of tomato yellow leaf curl virus. Journal of Economic Entomology 112, 2790–2796.Google ScholarPubMed
Zheng, HX, Xie, W, Fu, BL, Xiao, S, Tan, X, Ji, Y, Cheng, JX, Wang, R, Liu, BM, Yang, X, Guo, ZJ, Wang, SL, Wu, QJ, Xu, BY, Zhou, XM and Zhang, YJ (2021) Annual analysis of field-evolved insecticide resistance in Bemisia tabaci across China. Pest Management Science 77, 2990–3001.10.1002/ps.6338CrossRefGoogle ScholarPubMed
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